Visual, Somatosensory, and BimodalActivities in the Macaque ParietalArea PEc

Rossella Breveglieri, Claudio Galletti, Simona Monaco and

Patrizia Fattori

Dipartimento di Fisiologia Umana e Generale, Piazza di Porta

San Donato, 2, I-40126 Bologna, Italy

Caudal area PE (PEc) of the macaque posterior parietal cortex hasbeen shown to be a crucial node in visuomotor coordination duringreaching. The present study was aimed at studying visual andsomatosensory organization of this cortical area. Visual stimula-tions activated 53% of PEc neurons. The overwhelming majority(89%) of these visual cells were best activated by a dark stimuluson a lighter background. Somatosensory stimulations activated 56%of PEc neurons: most were joint neurons (73%); a minority (24%)showed tactile receptive fields, most of them located on the arms.Area PEc has not a clear retinotopy or somatotopy. Among the cellstested for both somatosensory and visual sensitivity, 22% werebimodal, 25% unimodal somatosensory, 34% unimodal visual, and19% were insensitive to either stimulation. No clear clustering ofthe different classes of sensory neurons was observed. Visual andsomatosensory receptive fields of bimodal cells were not in reg-ister. The damage in the human brain of the likely homologous ofmacaque PEc produces deficits in locomotion and in whole-bodyinteraction with the visual environment. Present data show thatmacaque PEc has sensory properties and a functional organization inline with the view of an involvement of this area in those processes.

Keywords: body-world interaction, dorsal visual stream, locomotion,multisensory, somatotopy

Introduction

Caudal area PE (PEc), corresponding to the caudal part of

cytoarchitectural field PE, has been traditionally seen as a

somatosensory association area of the posterior parietal cortex

(Pandya and Seltzer 1982). Recent studies have shed light on the

functional properties of PEc neurons, including the demonstra-

tion of cells with visual responses to moving light bars

(Battaglia-Mayer et al. 2001; Ferraina et al. 2001; Squatrito

et al. 2001) and optic flow stimuli (Battaglia-Mayer et al. 2001;

Raffi et al. 2002), cells modulated by passive somatosensory

inputs (mainly from the arm) (Breveglieri et al. 2006), as well as

arm-reaching cells (Batista et al. 1999; Battaglia-Mayer et al.

2001; Ferraina et al. 2001) and cells modulated by oculomotor

activity (Battaglia-Mayer et al. 2001; Ferraina et al. 2001).

According to the results of these studies, it has been suggested

that PEc is a visuomotor area involved in creating and

maintaining an internal representation of one’s own body

(Breveglieri et al. 2006). This area is part of a mosaic of areas

likely involved in early stages of motor programming, where

inputs coming from eye and hand are integrated to control arm

movements toward targets in the peripersonal space (Batista

et al. 1999; Battaglia-Mayer et al. 2001; Ferraina et al. 2001). This

hypothesis is supported by connectional studies (Johnson and

Ferraina 1996; Matelli et al. 1998; Marconi et al. 2001) according

to which the caudal part of the superior parietal lobule is

directly connected with dorsal premotor areas containing cells

modulated by arm position and arm direction of movement

(Caminiti et al. 1991), as well as by eye position signals

(Boussaoud et al. 1998; Jouffrais and Boussaoud 1999).

Caudally to PEc, and bordering it, there is another visuomotor

area called V6A (Galletti, Fattori, Kutz, et al. 1999). Similarly to

PEc, area V6A contains visual (Galletti et al. 1996; Galletti,

Fattori, Kutz, et al. 1999) and somatosensory (Breveglieri et al.

2002) cells, as well as cells modulated by eye and armmovement

(Galletti et al. 1997; Fattori et al. 2001, 2005; Kutz et al. 2003).

Until recently, the anatomical proximity between V6A and PEc,

together with the functional similarities between the 2 areas,

has made it hard to assign recording sites to either of these

areas. This difficulty has been removed by a recent study

(Luppino et al. 2005) that provided cytoarchitectural criteria

to distinguish PEc from V6A, allowing to assign cells to either

areas on the basis of an objective criterion. We therefore

decided to reinvestigate visual and somatosensory properties

of PEc cells by assigning recording sites on the basis of the

architectural pattern of recorded brain region. We also in-

vestigated the existence in PEc of bimodal cells, sensitive to

both visual and somatosensory stimulations, and we checked

whether different sensory properties were spatially segregated

within PEc subregions.

Materials and Methods

Three normal adult Macaca fascicularis weighing between 3 and 7 kg

were used in this study. Data have been collected from 4 hemispheres.

Experiments were carried out in accordance with National laws on care

and use of laboratory animals and with the European Communities

Council Directive of 24 November 1986 (86/609/EEC), and were

approved by the Bioethical Committee of the University of Bologna.

A detailed description of training, surgical and recording procedures,

as well as of visual and somatosensory stimulations, anatomical re-

construction of recording sites and animal care are reported elsewhere

(Galletti et al. 1996; Galletti, Fattori, Kutz, et al. 1999; Breveglieri et al.

2006). Surgery to implant recording apparatus was performed in asepsis

and under general anesthesia (sodium thiopenthal, 8 mg kg h, i.v.).

Analgesics were used postoperatively (ketorolac trometazyn, 1 mg kg

i.m. immediately after surgery and 1.6 mg kg i.m. on the following days).

Extracellular recordings from area PEc were daily performed using

glass-coated metal microelectrodes with a tip impedance of 0.8--2

MOhms at 1 kHz. The monkeys were seated in a primate chair with

the head fixed. The recording chamber was filled with saline, a hydraulic

microdrive was tightly fixed on it and the electrode was advanced into

the brain through the intact dura using a 1 3 1-mm surface coordinate

system as a reference. Action potentials were sampled at 1 kHz. Each

animal was studied over a period of 4--8 months. During the last 2 weeks

of recordings, electrolytic lesions (30--40 lA cathodal current for 30 s)

were made at different depths along single penetrations carried out at

different coordinates within the recording chamber.

Cerebral Cortex April 2008;18:806--816

doi:10.1093/cercor/bhm127

Advance Access publication July 27, 2007

� 2007 The Authors

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permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

After the last recording session, the animals were anaesthetized with

ketamine hydrochloride (15 mg kg i.m.) followed by an i.v. lethal

injection of sodium thiopental and perfused through the left cardiac

ventricle with saline in phosphate buffer, and then with 4% para-

formaldehyde in phosphate buffer, followed by 5% glycerol in phos-

phate buffer. Electrode tracks and location of each recording site

obtained in the last 2 weeks were reconstructed on parasagittal (for 3

hemispheres) or coronal (for 1 hemisphere) sections of the brain on the

basis of marking lesions. Unmarked penetrations were located on brain

sections by interpolation with respect to penetrations with electrolytic

lesions, taking into account the coordinates of penetrations within

recording chamber. The locations of penetrations and depths of

recording sites were then checked with respect to the boundaries

between white and gray matter and the distance of recording site from

the surface of the hemisphere (Galletti et al. 1995, 1996, 2005).

Visual StimulationAnimals were trained to perform steady gaze fixation in a behavioral task

in which they had to look for 2--6 s at a small target rear-projected on

a large (80� 3 80�) tangent screen placed 57 cm from the eyes, ignoring

any other visual stimulus present or moving across the visual field.

Fixation was monitored with an infrared oculometer (Bach et al. 1983).

The fixation target could be projected in different positions on the

screen in order to allow visual stimulations even in the far periphery of

the visual field. A standard protocol was used for testing the visual

responsiveness of cells in record. Cells were first tested with ‘‘simple’’

visual stimuli: single light/dark borders, spots of light, light or dark bars

of different size, orientation, direction, and speed of movement rear-

projected on the screen facing the animal. If the neuron in record was

not responsive to these stimuli, testing was continued using more

complex patterns such as luminance gratings and corners of different

orientations, directions, and speeds of movement, shadows with

irregular contours, and shadows rapidly changing in size and/or shape.

If the cell was visually responsive, we mapped the borders of visual

receptive field with the stimulus eliciting the best response. In cases

where wewere not able to activate the unit with the visual stimuli above

described, we classified that unit as not visually responsive.

Somatosensory StimulationAnimals got used to be manipulated and touched on the whole body by

the experimenter, being rewarded with water and fruits during

manipulation. Neural activity was recorded while passive somatic

stimulations were applied on the whole body according to the standard

protocol described in Breveglieri et al. (2002, 2006). The first somato-

sensory stimuli applied consisted of hair deflections by cotton flacks,

touch or light pressure of the skin. If no responses were elicited, we

attempted deep pressure in order to stimulate subcutaneous tissues

(deep tactile stimulation), and finally slow and fast passive rotations of

limb joints (proprioceptive stimulation).

In order to exclude visual influences, somatosensory stimulations

were performed in complete darkness. The experimenter stood behind

the animal and delivered stimuli on both sides of the body. Eye position

and movement were monitored to exclude the possibility that observed

modulations were due to oculomotor activity.

When a neuron responded to a somatosensory stimulation, it was clas-

sified as either tactile or sensitive to joint rotation, depending on the stim-

ulus required. Otherwise, the cells were classified as nonsomatosensory.

Bimodal Visual/Somatosensory ActivitySingle PEc neurons underwent both somatosensory and visual stimula-

tions in an order that was randomized across cells. According to the

results of these tests, neurons were classified in 4 groups: bimodal,

unimodal somatosensory, unimodal visual, unresponsive.

Among bimodal cells, we checked whether visual and somatosensory

receptive fields were in register or not. We also compared visual

properties of bimodal neurons with those of strictly unimodal visual, as

well as somatosensory properties of bimodal neurons with those of

unimodal somatosensory neurons.

Cytoarchitectural AssessmentAnalysis of Nissl-stained sections allowed us to recognize whether

recording sites were within the limits of area PEc. Recording sites were

assigned to area PEc according to the cytoarchitectural criteria de-

scribed in Pandya and Seltzer (1982) and Luppino et al. (2005). Briefly,

area PEc is characterized by the presence of a clear size gradient in layer

III, which is densely populated by medium-sized pyramids in its lower

part, and by a dense layer V with a high number of relatively large

pyramids. On the basis of these and other more subtle cytoarchitectural

criteria, area PEc is clearly distinguishable from the neighboring areas

medial intraparietal area (MIP), medial area PG (PGm), V6A, and PE, as

detailed in Luppino et al. (2005).

Two-dimensional and Three-dimensional Cortical MapsThree-dimensional (3-D) and 2-dimensional (2-D) surface-based recon-

structions of the studied brains were done using the software CARET

(http://brainmap.wustl.edu/caret Van Essen et al. 2001 see Fig. 1). The

reconstructions were made starting from cortical mid-thickness con-

tours of brain sections spaced 300 lm apart. The contours were

imported in CARET, together with the location of cytoarchitectonic

borders of area PEc, and manually aligned to obtain a smoothed 3-D

reconstruction and a flattened map of the brain (for details, see Galletti

et al. 2005).

To draw the average outline of area PEc (shown in Fig. 1), we reported

the borders of PEc with nearby areas V6A, MIP, PE, PGm of single cases

on the atlas brain (http://brainmap.wustl.edu/caret). The borders with

PE rostrally and V6A caudally were better defined in cases cut in sagittal

plane, whereas the borders with PGm medially and MIP laterally were

better defined in cases cut in coronal plane.

Electrophysiological data were reported on 2-D maps of the brains

reconstructed as described in detail in (Galletti, Fattori, Kutz, et al. 1999;

Breveglieri et al. 2006). We built a summary 2-D map of the 4

hemispheres we studied, mirroring the maps of the right hemispheres

on those of the left hemispheres, and aligning the individual maps on the

cytoarchitectonic PEc/V6A border and on the interhemispheric fissure.

Results

We recorded the activity of 198 PEc cells in 4 hemispheres of 3

animals.

Figure 1 shows the average extension of the cytoarchitectoni-

cally defined area PEc (Pandya and Seltzer 1982; Luppino et al.

2005) on 3-D (Fig. 1A) and 2-D (Fig. 1B) reconstructions on the

monkey atlas brain. PEc is located in the caudalmost third of

the superior parietal lobule. It extends from the caudal tip of the

cingulate sulcus anteriorly, to the parieto-occipital sulcus

posteriorly, and from the medial surface of the brain to the

medial bank of intraparietal sulcus. The brain location of area

PEc was similar across single cases.

Visual Cells

Of the 146 neurons tested for visual sensitivity, 77 cells (53%)

were responsive to visual stimulation. For 64 out of 77 visual

cells we were able to determine the most effective visual

stimulus among the battery tested; the remaining 13 cells were

lost before finishing the testing protocol, and were excluded

from subsequent analyses.

A consistent finding in our experiments was that PEc visual

cells tended to show stronger visual responses to dark stimuli

moved against a lighter background, in comparison with stimuli

of the opposite polarity. All visual stimulations were performed

while the animals were fixating. Figure 2 shows examples of

visual responses obtained with different types of stimuli. The

unit in Figure 2A was responsive to a simple stimulus (dark bar)

moving to and fro across its visual receptive field. A dark bar

correctly oriented andmotionless within the receptive field was

also effective in activating the cell (not shown in the figure).

The orientation of moving bar was a critical factor. The cell was

weakly responsive to bars oriented at 45� from the preferred

Cerebral Cortex April 2008, V 18 N 4 807

orientation (the vertical), and was completely silent for bars

oriented 90� from the preferred orientation.

Cell in Figure 2B showed a strong response to a dark bar, like

that in Figure 2A, but, differently from it, the discharge was

modulated by the direction of motion. This neuron was also

responsive, although less strongly, to a light bar of the same

orientation and direction of movement as the dark bar. The cell

was also weakly modulated by a dark square expanding against

a lighter background, whereas it did not respond to stimulus

contraction.

Cell in Figure 2C was strongly responsive to complex

stimulations. Simple stimuli (like light/dark borders or spots)

activated only weakly the cell (not shown in the figure). Hand

shadows waved across the receptive field were particularly

effective, as shadows of elongated objects moving across the

receptive field along their main axis of elongation. The cell

showed a certain degree of orientation sensitivity, as vertical

objects moved vertically evoked stronger responses than

horizontal objects moved horizontally. Objects which moved

perpendicularly to their main axis of elongation were

not effective in modulating cell activity (not shown in the

figure), contrary to what was observed in the unit illustrated in

Figure 2A,B.

Cell in Figure 2D was another example of unit responsive to

complex stimulation, but much less responsive, or not at all, to

simple stimuli. It was activated by a dark square expanding

within the receptive field, whereas a dark bar moved across the

receptive field evoked a poor response, and no response at all

was evoked by light bars moving with different orientations in

different directions across the receptive field.

We found that the overwhelming majority (n = 57/64; 89%) ofPEc visual cells were best activated by dark stimuli (bars, spots,

or shadows of different shapes). A minority of cells was equally

activated by dark and light stimuli, but none of the cells of our

sample preferred light stimuli moving against a darker back-

ground. About 30% (n = 20/64) of the PEc visual cells gave

similar responses for different visual stimuli among those we

tested, whereas the majority (n = 44/64) were selective for the

stimulus type. Among these latter, 20% preferred simple stimuli

(like neurons A and B in Fig. 2), whereas 80% preferred complex

stimuli, like the neurons C and D in Figure 2. Often, cells

preferred complex stimuli moved across the receptive field at

a continuously varied speed, orientation, and/or direction,

which avoided adaptation of cell discharge.

Receptive-field size increased with eccentricity in area PEc,

and was on average larger than that of cells sampled in the

nearby area V6A (see Fig. 3A; Galletti, Fattori, Kutz, et al. 1999).

Regression lines from the 2 areas were significantly different

one to another (1-way analysis of covariance, P < 0.01).

Both central and peripheral (up to about 70�) parts of the

visual field are represented in PEc (gray area Fig. 3B). Although

the contralateral hemifield is the most represented, a few

receptive fields were also found in the ipsilateral part of the

visual field, near the vertical meridian. Upper and lower

contralateral quadrants are both well represented.

Cells preferring simple stimuli, complex stimuli, and non-

selective cells represented more or less the same part of the

visual field (Fig. 3B), though the receptive fields of cells

selective for simple stimuli were all centered at eccentricities

higher than 20� (Fig. 3C).

Visual Topography

We analyzed the distribution of receptive-field locations on

bidimensional representations of the cortical region we studied.

As evident in the Figure 4A, the contralateral hemifield was

represented everywhere within PEc. Cells representing the

vertical meridian, the horizontal meridian, the upper or lower

quadrants, and the ipsilateral hemifield were randomly scat-

tered throughout PEc without any evidence of spatial segrega-

tion (Fig. 4A). Similarly, receptive fields with different

eccentricities were not orderly distributed within PEc (Fig.

4B), confirming the overall impression of a nontopographic

representation of the visual field.

Figure 1. Brain location of area PEc. (A) Dorsomedial, medial, and dorsal 3-D views of the surface-based reconstruction of the atlas brain. (B) 2-D reconstruction of the atlas brain.The average extent and location of the cytoarchitectonically defined area PEc is outlined on each reconstruction. Location of areas V6 and V6A is also shown. Abbreviations: Cal5calcarine fissure; Cin5 cingulate sulcus; Cs5 central sulcus; IPs5 intraparietal sulcus; Ls5 lunate sulcus; POs5 parieto-occipital sulcus; POm5medial parieto-occipital sulcus;STs5 superior temporal sulcus; Syl5 Sylviane fissure. A5 anterior; V5 ventral; L5 lateral; P5 posterior; M5 medial; V65 area V6 (Galletti, Fattori, Gamberini, et al. 1999);V6A 5 area V6A (Galletti, Fattori, Kutz, et al. 1999); PEc 5 area PEc (Pandya and Seltzer 1982).

808 Sensory Properties in Macaque Area PEc d Breveglieri et al.

One could argue that the process of pooling data from

different cases on the same 2D map could hide visual top-

ographies present in single cases. Although data from single

cases were typically not sufficient to establish a possible visual

topography in PEc, or lack thereof, they can help in visualizing

the extent of visuotopic order in small portions of this area. To

this effect we analyzed sequences of receptive fields encoun-

tered during individual electrode penetrations, as illustrated in

Figure 5 for 2 penetrations carried out in 2 hemispheres of one

single monkey. The right hemisphere was cut sagittally (Fig. 5A)

and the left hemisphere coronally (Fig. 5B). Looking at the

sequence of the receptive-field locations found in penetration

a (lower part of Fig. 5A), it is evident that we encountered

a large scattering of receptive fields, which included scatters

from ipsi to contralateral visual field (e.g., receptive fields 2--3),

as well as from upper to lower visual field (receptive fields 4--5).

Note that cells 2 and 3 were only 95 lm apart one from the

other, and cells 4 and 5 were 210 lm apart. The total distance

between cells 2 and 5 was about 500 lm: in this small region of

cortex, 3 of the 4 quadrants of the visual field were represented.

The same result arises from the analysis of receptive-field

sequence of penetration b, shown in the bottom part of Figure

5B. Moving the microelectrode a few tens of microns within the

cortex, receptive fields ‘‘jumped’’ from lower to upper quadrant

(receptive fields 3--4), and from periphery to central part of the

visual field (receptive fields 6--7).

In summary, small regions of PEc yielded receptive fields that

covered large portions of the visual field, apparently obeying no

visuotopic order, and hence confirming the results obtained

with the cumulative 2-D reconstructions of visual data.

Somatosensory Cells

The functional characteristics of PEc cells responding to passive

somatosensory stimulation have been recently reported in

a separate paper (Breveglieri et al. 2006). There, we found

that 56% of cells (n = 83/147) were modulated by passive

somatosensory stimulation. The majority of these (73%, n = 60)

responded to joint rotations, whereas 24% responded to tactile

stimulation (Fig. 6A,B). Joint-modulated cells were mostly

activated by rotation of the upper limbs (82%). The majority

of tactile receptive fields (61%) were located on the arms or on

nearby regions of the trunk. A minority were located on the legs

and on the rest of the trunk. The large majority of somatosen-

sory responses (90%) were evoked by contralateral stimulation

(Fig. 6C), but no somatotopic organization was apparent.

Somatosensory cells, somatosensory submodalities, and body

part representations were not clustered in PEc subregions (Fig.

6D), as better clarified by 2 exemplary groups of nearby cells

reported in Figure 6E. Here we show that small areas in PEc

contain somatosensory cells with receptive fields located in

parts far away from each other on the body (from shoulder to

hip, example 1, or from back to wrist, example 2). Here again, as

also shown for PEc visual organization, a lack of topographic

order is apparent.

Bimodal Visual and Somatosensory Cells

Neurons tested with both visual and somatosensory stimula-

tions were divided in 4 categories: 34% (n = 32) were unimodal

visual units, 25% (n = 23) were unimodal somatosensory units,

22% (n = 21) were bimodal units, and 19% were not driven by

any of the sensory stimuli attempted in the present study.

No evident differences were found in the visual features of

unimodal and bimodal cells, as shown in Figure 7. The

represented visual field (Fig. 7A,C) and the relationship between

eccentricity and the receptive-field size (Fig. 7B,D) are similar in

these 2 groups of cells. The figure also shows that the visual

Figure 2. Responses of PEc cells to different types of visual stimuli. (A, B) neuronspreferring simple stimuli; (C, D) neurons preferring complex stimuli. Each inset contains, fromtop to bottom, schematic representation of the stimulation of the receptive field (dashed line),peri-event time histogram, bar indicating the duration of visual stimulation, random-dotdisplay of spikes recorded during each trial, recordings of horizontal and vertical componentsof eye positions. (A) Responses of a cell to moving dark bars with different orientations. (B)Responses of a cell to a moving dark bar, to moving light bars, and to expanding--contractingdark square; (C) activity of a PEc cell to hand shadows repeatedlywaved across the receptivefield (left), to moving dark bars with different orientations moved repeatedly on the receptivefield and entering with the short side (center and right); (D) activity of a cell to expanding--contracting dark square, and to moving dark and light bars with different orientations. Binwidth5 20 ms; eye traces: scalebar, 60�; vertical scales on histograms: (A) 65 spikes/s; (B)40 spikes/s; (C) 100 spikes/s; (D) 35 spikes/s.

Cerebral Cortex April 2008, V 18 N 4 809

features were similar to those of the total population of PEc

visual cells.

Figure 8 summarizes the somatosensory properties of unim-

odal and bimodal cells of area PEc. Unimodal somatosensory

cells have receptive fields that cover a similar range of body

parts as the total population of PEc somatosensory cells

(compare Fig. 8A with Fig. 6A). Also the preference of joint

versus tactile stimulation (Fig. 8B) and the bias toward the

contralateral part of the body (Fig. 8C) are very similar in

unimodal and total cell population (see Fig. 6B,C).

Similarly to unimodal somatosensory, in bimodal neurons,

somatosensory tactile receptive fields and joints modulating

cell’s activity were mostly located on upper limbs (Fig. 8D).

We did not find any bimodal cell modulated by somatosensory

stimuli with a receptive field on distal parts of the limbs,

contrary to what observed in the unimodal somatosensory cells

(see Fig. 8A). Bimodal cells could be modulated by passive joint

rotation or by tactile stimulations in almost the same percent-

age (Fig. 8E), again in contrast with unimodal somatosensory

cells that clearly preferred joint rotations (see Fig. 8B). Similarly

to unimodal somatosensory cells, instead, the majority (90%)

of somatosensory receptive fields of bimodal cells was located

on the contralateral side of the body (compare Fig. 8F with

Fig. 8C).

No systematic relationship was found in bimodal cells be-

tween the location of visual and somatosensory receptive fields,

contrary to what observed in another visuo-somatosensory area

containing bimodal cells (ventral intraparietal area [VIP],

Duhamel et al. 1998). For instance, PEc cells with somatosensory

receptive fields located on the shoulder, could have visual

receptive fields located in either central, peripheral, contralat-

eral, or ipsilateral part of the visual field (see Fig. 9A). In turn, cells

with the visual receptive field in the same part of the visual field

could have the somatosensory receptive field in different parts of

the body (see Fig. 9B--D).

Figure 10 shows the distribution of unimodal and bimodal

cells within area PEc. Visual and somatosensory cells are mixed

together, but it is quite evident that they are distributed along

a medio/lateral visuo-somatic trend, with the visual cells more

concentrated in the postero-medial part of the area and the

somatosensory cells in the antero-lateral part of PEc; bimodal

visual/somatic cells are distributed in between. Apart from this

trend, no clear clustering of sensory properties was observed,

and in several recording sites we found cells with different

functional properties one near to another.

ips

A

B

Figure 4. Visual organization of area PEc. (A) Representation of ipsilateral andcontralateral hemifields (left), and of upper and lower hemifields (right), on a flat mapof the caudal pole of the superior parietal lobule. Data from 4 hemispheres aresummarized in each map. Different symbols indicate PEc cells whose receptive-fieldcenters were in different parts of the visual field, as indicated at the top left part ofeach map. Location of each symbol in the map represents the location of each cell inarea PEc. Receptive fields centered on the fovea were not considered. Maps fromdifferent cases were aligned posteriorly on the border between PEc and V6A, andmedially on the interhemispheric line (see symbols[\on the maps and on the brainsilhouette to the right; scale5 1 mm/division). Dashed lines on the anterior part of themaps indicate the cytoarchitectural borders between areas PEc and PE in single cases.(B) Eccentricity representation. White, gray, and black indicate PEc cells withreceptive-field centers at different eccentricities, as indicated on the top left. PE5areaPE (Pandya and Seltzer 1982). Other abbreviations as in Figure 1.

A B C

Figure 3. Visual cells of area PEc. (A) Receptive-field size versus eccentricity. Regression plot of receptive-field size (square root of area) against eccentricity for 55 PEc visual cells.The regression equation is receptive-field size5 27.65�þ 0.31793 eccentricity; regression line for V6A visual cells (dashed line) is reported for comparison (receptive-field size521.0�þ 0.223 eccentricity, see Galletti, Fattori, Kutz, et al. 1999). (B) Gray area indicates the total visual-field representation in area PEc, dotted line the visual-field represented bycells selective for simple stimuli, continuous line and dashed line those represented by cells selective for complex stimuli and for cells nonselective for the shape of visual stimulusrespectively. Ipsi 5 ipsilateral visual field; contra 5 contralateral visual field. (C) Distribution of receptive fields centers of cells preferring simple (filled circles, N 5 7), complex(empty circles, N 5 24) stimuli, and cells nonselective for the stimulus shape (crosses, N 5 14). Dashed line outlines the central 20� of the visual field.

810 Sensory Properties in Macaque Area PEc d Breveglieri et al.

Discussion

In the present study we characterized visual, somatosensory,

and bimodal cells in area PEc, taking advantage of recently

established cytoarchitectonic criteria to assign recording sites

to this area (Luppino et al. 2005). Over half of the PEc cells were

sensitive to visual stimulation, these being maximally activated

by dark stimuli moving in a light background, as it is typically the

case in natural scenes (Bex and Makous 2002). Moreover, the

majority of cells required relatively complex, and dynamic visual

stimuli for strong responses. Although analysis of the receptive

fields of visual cells suggested that these were not retinotopi-

cally organized, receptive fields of adjacent neurons typically

overlapped at least partially, showing no evidence of map

discontinuities, as typically observed in occipital visual areas

(Rosa 2002). Thus, the overall lack of visual topography may be

the result of a large amount of receptive-field scatter, pro-

portional to the large size of single cell receptive fields (Hubel

and Wiesel 1974).

The lack of visual topography, together with the large

receptive-field size, certifies the position invariance of the visual

representation in PEc. It remains that in area PEc, even a broad,

large-scale visuotopic order, showing at least different areal

locations mirroring different visual-field quadrant representa-

tions, is apparently absent. The absence of a visuotopic order,

together with the continuity of visual map in nearby neurons,

suggests that PEc elaborates visual information for a functional

purpose which nothing has to do with the representation of the

visual field as it is.

PEc has a high proportion of visual cells and also of

somatosensory cells. The majority of somatosensory neurons

responded to joint rotations, and a minority to tactile stimula-

tions. There was no evidence of somatotopic organization. We

found a polymodal convergence (visual and somatosensory) in

22% of PEc cells. We found a puzzling lack of systematic

relationship between visual and somatosensory input onto

single PEc cells. These bimodal cells were mixed with unimodal

visual and unimodal somatosensory neurons without any

evident sign of a spatial pattern of segregation. However, we

observed a gradient of sensory inputs across PEc with more

somatic input rostrally and laterally and more visual input

caudally and medially.

Visual and Somatosensory Sensitivities in Area PEc

Recent studies (Battaglia-Mayer et al. 2001; Squatrito et al. 2001)

have reported the presence of visual neurons in area PEc in

percentages (65% and 45%, respectively) not dissimilar from the

one we found in the present work. Results are remarkably

similar, in particular if we take into account the different stimuli

used (light bars in previous studies vs. light and dark stimuli in

present report), the different extents of visual field tested

Figure 5. Visual representation in single penetrations carried out in area PEc. (A, B) Top: Parasagittal (A) and coronal (B) sections of 2 hemispheres of one case, taken at the levelsshown on brain silhouette below. a and b show the reconstruction of 2 microelectrode penetrations carried out in PEc. Bottom: Visual receptive-field sequence of neuronsencountered in each penetration. Cells are numbered progressively along the penetration track (shown aside each receptive-field sequence). Abbreviations as in Figures 1, 3, and 4.

Cerebral Cortex April 2008, V 18 N 4 811

(central 30� in previous studies vs. virtually the entire visual field

here), and the location and extent of recording sites (the

medialmost part of PEc in previous studies vs. the full extent of

PEc here). Also in agreement with previous reports is the

absence of a retinotopic map (Battaglia-Mayer et al. 2001;

Squatrito et al. 2001).

Present data suggest that visual cells are not uniformly

distributed across the area, showing an increasing gradient

toward the postero-medial part of PEc. Such a gradient-like

organization is relatively common in high-order sensory associ-

ation areas, including for example the inferior temporal cortex

(Rosa and Tweedale 2005).

Thanks to the sensitivity of several PEc visual cells to

contracting/expanding optic flow stimuli, with a strong di-

rectional tuning (Raffi et al. 2002), it was suggested that PEc can

code heading movements during locomotion. Present data on

PEc visual responsiveness to complex visual stimuli (continu-

ously moving and changing in size) support this hypothesis. This

plausible role in controlling body stance during locomotion was

suggested also for dorsomedial area (DM) of the marmoset (Lui

et al. 2006), an area likely homologous to macaque area V6

(Rosa and Tweedale 2001, 2005). We suggest that area V6, rich

in direction selective cells (Galletti, Fattori, Gamberini, et al.

1999), sends directional visual inputs for motor control to PEc

through area V6A (Galletti et al. 2001) and thus enables PEc to

perform visual analyses during locomotion.

Even the complete representation of inferior and superior

contralateral quadrants up to the far periphery seen in PEc

(present results) supports the view of a role for this area in

locomotion, as in locomotion the entire visual environment

sweeps across the retina, and PEc visual cells seem to be well

equipped to evaluate visual information in that situation.

Visually induced self-motion (vection) requires wide stimuli

that are perceived as emanating from a distance (Dichgans and

Brandt 1978; Delorme and Martin 1986; Howard and Heckmann

1989; Previc and Neel 1995). Thus, only those visual areas

whose neurons have extremely large receptive fields and with

a complete representation of the visual field up to the far

periphery (like PEc, see Fig. 3) can qualify as the site of vection

and other ambient visual processes.

In humans, there is a stronger parieto-occipital activation for

expanding than for receding optical flow (Tootell et al. 1996).

This same preference has been found in monkey area PEc (Raffi

et al. 2002) and anecdotically confirmed here (see the examples

of Fig. 2B--D with stronger responses to enlarging than to

contracting visual stimuli). These data together suggest that it is

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Figure 6. Somatosensory representation in area PEc. (A) Locations of somatosensory receptive fields in PEc: joints (black dots) and tactile receptive fields (thick lines drawn on theanimal body). The size of each dot is proportional to the number of modulated units. All somatosensory receptive fields have been reported on the left side of the body. (B) Incidenceof joint and tactile cells. (C) Incidence of contralateral (contra), ipsilateral (ipsi), and bilateral modulations. (D) Cortical distribution of PEc somatosensory cells. Bottom: Flattenedsummary map of the dorsal exposed surface of PEc showing the cortical distribution of somatosensory representation. Dashed lines labeled with numbers 1 and 2 encircle 2 groupsof cells whose somatosensory receptive fields are located where illustrated in the monkey silhouettes in (E). It is evident that cells in nearby parts of the cortex had somatosensoryreceptive fields in different parts of the body. Abbreviations as in Figures 1 and 4.

812 Sensory Properties in Macaque Area PEc d Breveglieri et al.

plausible that PEc is involved in perception and/or in visually

guided motor control of forward locomotion, which is of course

more common with respect to backward locomotion in humans

and monkeys.

The mixture of visual and somatosensory neurons observed in

PEc, and the presence of bimodal visual/somatosensory cells as

well, suggest a complementary regional integration within the

area between the 2 sensory modalities. As the somatosensory

activity is mainly referred to the limbs, this integration between

visual and somatosensory information appears useful to co-

ordinate motor activity during locomotion, particularly when

one moves in a complex visual environment which requires

a continuous interaction between body parts (upper limbs,

trunk, lower limbs) and objects in the visual world. The

particular sensitivity of these visual cells to stimuli continuously

changing in form, size, and speed (present results), together

with the presence in this same area of somatosensory cells

sensitive to joint rotations or tactile stimulations (present

results and Breveglieri et al. 2006) and of reach-related neural

activity (Batista et al. 1999; Fattori et al. 2000; Battaglia-Mayer

et al. 2001; Ferraina et al. 2001), fully agree with this view.

During locomotion, the brain has to relate body movements

with the flow of visual information coming from the entire

visual environment. The analysis of visual scene during loco-

motion is different from that required during prehension of

small objects. In grasping an object, we need specific informa-

tion about features and spatial location of that object, and the

fact that visual and somatosensory receptive fields are in register

could be useful in that process. In visually guided locomotion

this need is less compelling, given the more global interaction

between body and visual environment. Thus, the nontopo-

graphic and nonregistered organization of visual and somatic

information, as well as the interaction between these 2 inputs

upon single cells observed in PEc seem to be in line with the

suggested functional role of this area.

Another support for the role here suggested for PEc is

provided by a case study (Kase et al. 1977) reporting topograph-

ical disorientation and abnormalities of body movement after

damage of the posterior part of the superior parietal lobule,

a region of the brain likely containing the homolog of monkey

area PEc. The patient in the long period was not particularly

impaired in reaching and grasping objects under visual guidance,

but she was impaired in the whole-body interaction with a goal

object in the surrounding visual world, like in lying in the

appropriate way on a bed, or in modifying her body posture in an

appropriate way in order to sit on a chair. Kases’s patient showed

long lasting behavioral abnormalities in whole-body movements

for interacting with the visual environment. These functions,

lost in Kase’s patient due to the lesion in a region likely homolog

to monkey area PEc, seem to be supported by the results

reported here and in other studies about PEc, and strongly

support the role of PEc in controlling locomotion and whole-

body interactions with the visual environment.

More recent studies of human brain imaging reported

activations in dorsomedial parietal regions of the brain likely

including the human homologous of area PEc, in experiments

where the subjects had to use vision in order to judge self-

motion or to guide locomotion, to control postural balance, to

guide vehicles (De Jong et al. 1994; Tootell et al. 1996; Brandt

et al. 1998; Kleinschmidt et al. 2002). It remains unclear

whether this brain region could be considered as the human

homolog of area PEc, or the homolog of the neighboring area

V6A, or even whether it includes both areas or even other

neighboring areas with similar functional characteristics. Fur-

ther experiments are needed to verify this point.

Is PEc an Independent Functional Area?

Area PEc contains both visual and somatosensory cells. The

same kinds of cells are also contained in areas V6A (Galletti et al.

1996; Galletti, Fattori, Kutz, et al. 1999; Breveglieri et al. 2002)

and MIP (Colby and Duhamel 1991; Klam and Graf 2003), with

which PEc shares borders in the caudal part of the superior

parietal lobule. Thus, the question might arise of whether PEc is

an independent cortical area or is part of the nearby areas V6A

and MIP. Another possibility is that these subdivisions have

relatively indistinct borders, merging gradually into each other.

The main arguments in favor of PEc as an independent area are

centered on its distinctive architecture (Luppino et al. 2005)

and a different set of anatomical connections (Johnson and

Ferraina 1996; Matelli et al. 1998; Marconi et al. 2001).

Moreover, despite some similarities in functional properties,

there are also functional differences. For instance, visual re-

ceptive fields of PEc cells are on average larger than those of

V6A cells for a same given eccentricity (see Fig. 3A), and a lower

percentage of PEc cells shows strong responses to simple visual

stimuli such as bars and spots, in comparison with V6A (see

Galletti et al. 1996; Galletti, Fattori, Kutz, et al. 1999). Visual cells

of area MIP are insensitive to the direction of movement of

visual stimuli (Colby and Duhamel 1991), whereas almost all PEc

Figure 7. Visual properties of unimodal and bimodal PEc cells. (A, C) Continuous line:Visual-field representation of unimodal visual (A) and bimodal (C) cells; gray area:visual-field representation of all PEc visual cells (see Fig. 3). (B, D) Receptive-field(square root of area) size versus eccentricity for unimodal (B) and bimodal (D) cells(continuous lines). The regression equation is receptive-field size 5 23.03� þ 0.40513 eccentricity for unimodal cells (N5 24); receptive-field size5 28.50�þ 0.25293eccentricity for bimodal cells (N 5 15). For comparison, regression line of PEc visualcells (dashed line) is also reported (see Fig. 3). Other conventions as in Figure 3.

Cerebral Cortex April 2008, V 18 N 4 813

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Figure 8. Somatosensory properties of unimodal and bimodal PEc cells. (A, D) Locations of joints (black dots) and of tactile receptive fields (thick lines drawn on the animal body) ofunimodal (A) and bimodal (D) cells. All somatosensory receptive fields have been reported on the left side of the body. (B, E) Incidence of proprioceptive and tactilemodulations for unimodal(B) and bimodal (E) cells; (C, F) incidence of contralateral, ipsilateral, and bilateral somatosensory modulations for unimodal (C) and bimodal (F) neurons. Conventions as in Figure 6.

A

B C D

Figure 9. Relationships between body and visual-field representations in bimodal PEc cells. (A) Visual receptive-field locations of 4 bimodal cells activated by somatosensorystimuli applied on the shoulder. (B--D) Locations of tactile receptive fields (thick lines drawn on the animal body) and joints (filled and open circles and crosses) modulating bimodalcells. Somatosensory receptive fields are represented with crosses, continuous and dashed lines according to the location of the visual receptive field, as indicated in the right upperpart of each inset. Cells having visual receptive field on the meridians were not considered. Other conventions as in Figures 3 and 6.

814 Sensory Properties in Macaque Area PEc d Breveglieri et al.

cells were direction selective (Squatrito et al. 2001). Finally, the

present data show that visual cells in PEc are more concentrated

in the postero-medial region of the area (see Fig. 10), at the

border with V6A, whereas visual cells in V6A are more

concentrated in the ventral part of the area (Fattori et al.

1999; Galletti, Fattori, Kutz, et al. 1999), at the opposite side

with respect to the border with PEc. The same is also true for

area MIP, which is known to contain a higher percentage of

visual cells in its ventral part (Colby and Duhamel 1991), far

from the border with PEc. In other words, the regions with the

highest number of visual cells in the 3 nearby areas PEc, V6A,

and MIP are not in continuity, as it would be perhaps expected if

these were parts of the same functional area.

The incidence of somatosensory cells in PEc (56%, present

results and Breveglieri et al. 2006) is higher than that in V6A

(32%, Breveglieri et al. 2002); the incidence of somatosensory

cells in area MIP has not yet been reported. PEc somatosensory

receptive fields are mostly located on the proximal parts of the

limbs (present results and Breveglieri et al. 2006), whereas in

V6A they encompass both proximal and distal parts of the arms

(Breveglieri et al. 2002), and in area MIP they are mostly located

on distal part of the arms (Colby and Duhamel 1991).

In summary, on balance, the evidence argues against PEc,

V6A, and MIP being part of a same cortical area. Recently, it was

proposed that the various primate posterior parietal areas

emerged as differentiations of a single somatotopic map

(Manger et al. 2002). Our data do not contradict this hypothesis,

given that the somatosensory receptive fields in PEc are more

proximal than those in area MIP (Colby and Duhamel 1991) and

in VIP (Duhamel et al. 1998), which become gradually more

located in distal limb (in MIP) or face (in VIP) as more lateral

parietal areas become involved. Also the different cytoarchitec-

tural patterns of these areas do not contradict this view, as in the

parietal areas of the ferret different cytoarchitectures in the

face versus body representations were found (Manger et al.

2002). In summary, the differences between PEc and more

lateral parietal areas could reflect functions related to different

body parts, without necessarily implying that these areas

perform very different neural operations. We believe that PEc

and the adjoining areas in superior parietal lobule mentioned so

far are different functional areas, some of them (like VIP) likely

mainly involved in the representation of the movements of

external objects toward some body parts, and others (like PEc,

V6A, and MIP) likely mainly involved in guiding body interaction

with the visual world.

Funding

European Union Commission (FP6-IST-027574-MATHESIS);

Ministero dell’Universita e della Ricerca; and Fondazione del

Monte di Bologna e Ravenna (Italy).

Notes

Authors wish to thank Roberto Mambelli, Leonida Sabattini, and

GiuseppeMancinelli for technical assistance; Dott.ssaMichelaGamberini

for cytoarchitectural analysis; Dott. Ivan Baldinotti for surface-based

reconstructions with CARET. We are grateful to Prof. Marcello Rosa for

helpful comments and corrections in themanuscript.Conflict of Interest:

None declared.

Funding to pay the Open Access publication charges for this article

was provided by FP6-IST-027574-MATHESIS.

Address correspondence to Prof. P. Fattori, Dipartimento di Fisiologia

Umana e Generale, Piazza di Porta San Donato, 2, I-40126 Bologna, Italy.

Email: patrizia.fattori@unibo.it.

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